Effects of lianas on forest biogeochemistry during their lives and afterlives.

Climate change and other anthropogenic disturbances are increasing liana abundance and biomass in many tropical and subtropical forests. While the effects of living lianas on species diversity, ecosystem carbon, and nutrient dynamics are receiving increasing attention, the role of dead lianas in forest ecosystems has been little studied and is poorly understood. Trees and lianas coexist as the major woody components of forests worldwide, but they have very different ecological strategies, with lianas relying on trees for mechanical support. Consequently, trees and lianas have evolved highly divergent stem, leaf, and root traits. Here we show that this trait divergence is likely to persist after death, into the afterlives of these organs, leading to divergent effects on forest biogeochemistry. We introduce a conceptual framework combining horizontal, vertical, and time dimensions for the effects of liana proliferation and liana tissue decomposition on ecosystem carbon and nutrient cycling. We propose a series of empirical studies comparing traits between lianas and trees to answer questions concerning the influence of trait afterlives on the decomposability of liana and tree organs. Such studies will increase our understanding of the contribution of lianas to terrestrial biogeochemical cycling, and help predict the effects of their increasing abundance.

Modelling the carbon balance in bryophytes and lichens: Presentation of PoiCarb 1.0, a new model for explaining distribution patterns and predicting climate-change effects.

PREMISE: Bryophytes and lichens have important functional roles in many ecosystems. Insight into their CO2 -exchange responses to climatic conditions is essential for understanding current and predicting future productivity and biomass patterns, but responses are hard to quantify at time scales beyond instantaneous measurements. We present PoiCarb 1.0, a model to study how CO2 -exchange rates of these poikilohydric organisms change through time as a function of weather conditions. METHODS: PoiCarb simulates diel fluctuations of CO2 exchange and estimates long-term carbon balances, identifying optimal and limiting climatic patterns. Modelled processes were net photosynthesis, dark respiration, evaporation and water uptake. Measured CO2 -exchange responses to light, temperature, atmospheric CO2 concentration, and thallus water content (calculated in a separate module) were used to parameterize the model's carbon module. We validated the model by comparing modelled diel courses of net CO2 exchange to such courses from field measurements on the tropical lichen Crocodia aurata. To demonstrate the model's usefulness, we simulated potential climate-change effects. RESULTS: Diel patterns were reproduced well, and the modelled and observed diel carbon balances were strongly positively correlated. Simulated warming effects via changes in metabolic rates were consistently negative, while effects via faster drying were variable, depending on the timing of hydration. CONCLUSIONS: Reproducing weather-dependent variation in diel carbon balances is a clear improvement compared to simply extrapolating short-term measurements or potential photosynthetic rates. Apart from predicting climate-change effects, future uses of PoiCarb include testing hypotheses about distribution patterns of poikilohydric organisms and guiding conservation strategies for species.

Smoothing out the misconceptions of the role of bark roughness in vascular epiphyte attachment.

Vascular epiphytes represent c. 10% of all vascular plant species. In epiphytes, attachment is essential for survival throughout consecutive ontogenetic stages of their life, starting with: (1) initial propagule attachment to the host; followed by (2) the development of first root-substrate connections; and (3) maintenance of this attachment despite increased size and mechanical disturbances by rain, wind, or crossing animals. Although structural dependence on a host is a defining characteristic of an epiphyte, the fundamental mechanism(s) of how these plants initially attach and remain attached to their hosts remain poorly understood. Bark characteristics such as stability and roughness have been highlighted as keys to an understanding of this connection. Here, we stress that the understanding of how an epiphyte attaches itself to the substrate is central for a meaningful quantification and interpretation of bark roughness. Without explicit information on the attachment mechanism or the relative sizes of the attaching structures, simply linking a haphazardly chosen index of bark roughness to epiphyte establishment is flawed. This review introduces a conceptual framework to explain the mechanistic link between epiphytes and host in different ontogenetic stages and should guide future work designed to improve our understanding of this vital part of epiphyte ecology.

Exo- and endophytic fungi enable rapid transfer of nutrients from ant waste to orchid tissue.

The epiphytic orchid Caularthron bilamellatum sacrifices its water storage tissue for nutrients from the waste of ants lodging inside its hollow pseudobulb. Here, we investigate whether fungi are involved in the rapid translocation of nutrients. Uptake was analysed with a 15 N labelling experiment, subsequent isotope ratio mass spectrometry (IRMS) and secondary ion mass spectrometry (ToF-SIMS and NanoSIMS). We encountered two hyphae types: a thick melanized type assigned to 'black fungi' (Chaetothyriales, Cladosporiales, and Mycosphaerellales) in ant waste, and a thin endophytic type belonging to Hypocreales. In few cell layers, both hyphae types co-occurred. 15 N accumulation in both hyphae types was conspicuous, while for translocation to the vessels only Hypocreales were involved. There is evidence that the occurrence of the two hyphae types results in a synergism in terms of nutrient uptake. Our study provides the first evidence that a pseudobulb (=stem)-born endophytic network of Hypocreales is involved in the rapid translocation of nitrogen from insect-derived waste to the vegetative and reproductive tissue of the host orchid. For C. bilamellatum that has no contact with the soil, ant waste in the hollow pseudobulbs serves as equivalent to soil in terms of nutrient sources.

A new approach to an old problem: how to categorize the habit of ferns and lycophytes.

BACKGROUND AND AIMS: Substrate preferences are often treated as species traits and are used to distinguish different habits, i.e. an epiphytic, lithophytic or terrestrial habit. Such a categorization, however, ignores substantial intraspecific variation. An approach that takes biological variability within a species into account is needed. METHODS: We focused on four large genera of ferns and lycophytes and found relevant information in >500 sources, such as online databases, checklists, floras and species descriptions. Translating textual information into a quantitative index, we quantified the propensity to grow on either substrate as a continuous trait for 1475 species. KEY RESULTS: Only a minority of species exhibited strict substrate fidelity, but a majority of them showed clear habitat preferences. The relative frequencies of intermediates between strict lithophytes, epiphytes and terrestrials does not support the frequent notion of ecological similarity of the lithophytic and epiphytic habitat. CONCLUSIONS: The compiled data are useful immediately for ecological and evolutionary studies with the focal taxa. More importantly, we propose the replacement of the concept of distinct habits with one of gradual differences. This should have a profound impact on any such study with plants in general.

CAM plants: their importance in epiphyte communities and prospects with global change.

BACKGROUND AND SCOPE: The epiphytic life form characterizes almost 10 % of all vascular plants. Defined by structural dependence throughout their life and their non-parasitic relationship with the host, the term epiphyte describes a heterogeneous and taxonomically diverse group of plants. This article reviews the importance of crassulacean acid metabolism (CAM) among epiphytes in current climatic conditions and explores the prospects under global change. RESULTS AND CONCLUSIONS: We question the view of a disproportionate importance of CAM among epiphytes and its role as a 'key innovation' for epiphytism but do identify ecological conditions in which epiphytic existence seems to be contingent on the presence of this photosynthetic pathway. Possibly divergent responses of CAM and C3 epiphytes to future changes in climate and land use are discussed with the help of experimental evidence, current distributional patterns and the results of several long-term descriptive community studies. The results and their interpretation aim to stimulate a fruitful discussion on the role of CAM in epiphytes in current climatic conditions and in altered climatic conditions in the future.

Holding on or falling off: The attachment mechanism of epiphytic Anthurium obtusum changes with substrate roughness.

PREMISE: For vascular epiphytes, secure attachment to their hosts is vital for survival. Yet studies detailing the adhesion mechanism of epiphytes to their substrate are scarce. Examination of the root hair-substrate interface is essential to understand the attachment mechanism of epiphytes to their substrate. This study also investigated how substrate microroughness relates to the root-substrate attachment strength and the underlying mechanism(s). METHODS: Seeds of Anthurium obtusum were germinated, and seedlings were transferred onto substrates made of epoxy resin with different defined roughness. After 2 months of growth, roots that adhered to the resin tiles were subjected to anchorage tests, and root hair morphology at different roughness levels was analyzed using light and cryo scanning electron microscopy. RESULTS: The highest maximum peeling force was recorded on the smooth surface (glass replica, 0 µm). Maximum peeling force was significantly higher on fine roughness (0, 0.3, 12 µm) than on coarse (162 µm). Root hair morphology varied according to the roughness of the substrate. On smoother surfaces, root hairs were flattened to achieve large surface contact with the substrate. Attachment was mainly by adhesion with the presence of a glue-like substance. On coarser surfaces, root hairs were tubular and conformed to spaces between the asperities on the surface. Attachment was mainly via mechanical interlocking of root hairs and substrate. CONCLUSIONS: This study demonstrates for the first time that the attachment mechanism of epiphytes varies depending on substrate microtopography, which is important for understanding epiphyte attachment on natural substrates varying in roughness.

The relationship between chlorophyllous spores and mycorrhizal associations in ferns: evidence from an evolutionary approach.

PREMISE: Approximately 14% of all fern species have physiologically active chlorophyllous spores that are much more short-lived than the more common and dormant achlorophyllous spores. Most chlorophyllous-spored species (70%) are epiphytes and account for almost 37% of all epiphytic ferns. Chlorophyllous-spored ferns are also overrepresented among fern species in habitats with waterlogged soils, of which nearly 60% have chlorophyllous spores. Ferns in these disparate habitat types also have a low incidence of mycorrhizal associations. We therefore hypothesized that autotrophic chlorophyllous spores represent an adaptation of ferns to habitats with scarce mycorrhizal associations. METHODS: We evaluated the coevolution of chlorophyllous spores and mycorrhizal associations in ferns and their relation to habitat type using phylogenetic comparative methods. RESULTS: Although we did not find support for the coevolution of spore type and mycorrhizal associations, we did find that chlorophyllous spores and the absence of mycorrhizal associations have coevolved with epiphytic and waterlogged habitats. Transition rates to epiphytic and waterlogged habitats were significantly higher in species with chlorophyllous spores compared to achlorophyllous lineages. CONCLUSIONS: Spore type and mycorrhizal associations appear to play important roles in the radiation of ferns into different habitat types. Future work should focus on clarifying the functional significance of these associations.

Island disharmony revisited using orchids as a model group.

One central concept in island biology is that island assemblages form subsets of the mainland species pool, being disproportionately rich or poor in certain taxonomic groups. This unbalanced composition, termed 'disharmony', is generally explained using a taxon-centred approach, linking the over- or under-representation of taxa to their colonisation abilities. However, islands may also harbour 'functionally' disharmonic flora, being disproportionately rich or poor in species with certain traits, which may offer greater insights into the processes driving island colonisation. Here, we use orchids as a model to illustrate key processes involved in the formation of functionally disharmonic island floras, including filtering effects (for example biotic interactions), and speciation. Our synthesis is based on a comprehensive orchid dataset of 27 637 species and combines both a literature review and simple exploratory analyses to show that orchids are significantly under-represented on islands relative to mainland regions and that insular orchids display shifts in functional traits, from the shortening of nectar spurs to facilitate ornithophily to changes in colour associated with generalist insect pollinators. We highlight that taxa are simply coarse proxies and that we need to consider species traits and interactions to gain a full understanding of the processes constraining plant assembly on islands.

Growth responses to elevated temperatures and the importance of ontogenetic niche shifts in Bromeliaceae.

Epiphytic bromeliads represent a major component of Neotropical forests, but the potential effect of climate change on these plants is unclear. We investigated whether and how bromeliads are affected by the predicted 3°C temperature rise by the end of the century. We conducted growth experiments with 17 epiphytic bromeliad species at different temperatures to determine their fundamental thermal niches. By comparing those with niches for germination, we tested whether ontogenetic niche shift or niche contraction occurs in Bromeliaceae. Applying a classical growth analysis, we assessed the relative importance of the underlying growth components on interspecific variations in growth. Members of two bromeliad subfamilies differed in their response to elevated temperatures: Tillandsioideae may be negatively affected, whereas Bromelioideae moved closer to their thermal optimum. Across different ontogenetic stages, thermal niche characteristics revealed both niche shift and niche contraction. Interspecific variation in growth was driven almost exclusively by net assimilation rate at all temperatures. We conclude that the vulnerability of tropical plants to a future increase in temperature may be more variable than suggested by previous studies. We emphasize the importance of assessing niche breadth over multiple life stages and the need for better microclimatic data to link laboratory data with field conditions.

Heteroblasty in epiphytic bromeliads: functional implications for species in understorey and exposed growing sites.

Background and Aims: The functional relevance of heteroblasty, an abrupt morphological change in the ontogeny of a considerable number of angiosperm species, is still largely unresolved. During the ontogeny of many epiphytic Tillandsioids (Bromeliaceae), such a change occurs when small individuals transform into larger, tank-forming individuals that are capable of external water storage. Apart from its fundamental effect on plant water relations, the associated transition from narrow to broader leaves also affects plant architecture. The morphological changes and their effect on light interception may be especially relevant for heteroblastic species in the moist understorey, which are expected to be limited primarily by light. Methods: A functional structural plant model (Yplant) was used to construct digital replicas of atmospheric and tank-forming individuals of four species, two of them naturally growing in exposed conditions and two occurring in understorey sites. This allowed the determination of leaf display efficiencies as well as a systematic analysis of leaf architectural traits and their effect on light interception. Key Results: Modifying existing plant morphologies showed that broader leaves cause more self-shading within the plant. This supports the hypothesis that species from the light-limited understorey benefit from the early atmospheric life form through increased light capture. Modelling plant morphology that continuously followed the ontogenetic trajectories of the leaf architectural traits revealed that the rising total leaf number in atmospheric individuals constantly increased self-shading. Therefore, at a certain ontogenetic stage, a tipping point was reached when the tank form was even favourable in terms of light capture as it was associated with fewer leaves. Conclusions: The effects of changes in leaf morphology and leaf architecture on plant light capture may explain the common occurrence of heteroblastic species in the understorey of Neotropical forests, which does not negate a simultaneous positive effect of heteroblasty on plant water relations.

The velamen radicum is common among terrestrial monocotyledons.

Background: The velamen radicum, a spongy and usually multiple-layered root epidermis composed of dead cells at maturity, is a textbook example of an adaptation that is typically associated with epiphytic orchids. Scope: Based on an extensive literature review, the occurrence of this structure was documented in approximately 240 genera of terrestrial monocotyledons (162 orchid and 74 non-orchid genera) and in one genus of dicotyledons. Mapping this character on a phylogenetic tree reveals that a velamen is found throughout the monocotyledons, ranging from members of early-branching Araceae to derived Cyperaceae. Conclusion: The current depiction of the velamen radicum in angiosperms and its almost exclusive association with the epiphytic lifestyle in orchids is misleading, which inevitably leads to a biased view of its evolution and function. The findings propose a re-evaluation of the occurrence, evolution and function of the velamen radicum in both terrestrial and epiphytic angiosperms.

Carbohydrate reserves in the facilitator cushion plant Laretia acaulis suggest carbon limitation at high elevation and no negative effects of beneficiary plants.

The elevational range of the alpine cushion plant Laretia acaulis (Apiaceae) comprises a cold upper extreme and a dry lower extreme. For this species, we predict reduced growth and increased non-structural carbohydrate (NSC) concentrations (i.e. carbon sink limitation) at both elevational extremes. In a facilitative interaction, these cushions harbor other plant species (beneficiaries). Such interactions appear to reduce reproduction in other cushion species, but not in L. acaulis. However, vegetative effects may be more important in this long-lived species and may be stronger under marginal conditions. We studied growth and NSC concentrations in leaves and stems of L. acaulis collected from cushions along its full elevational range in the Andes of Central Chile. NSC concentrations were lowest and cushions were smaller and much less abundant at the highest elevation. At the lowest elevation, NSC concentrations and cushion sizes were similar to those of intermediate elevations but cushions were somewhat less abundant. NSC concentrations and growth did not change with beneficiary cover at any elevation. Lower NSC concentrations at the upper extreme contradict the sink-limitation hypothesis and may indicate that a lack of warmth is not limiting growth at high-elevation. At the lower extreme, carbon gain and growth do not appear more limiting than at intermediate elevations. The lower population density at both extremes suggests that the regeneration niche exerts important limitations to this species' distribution. The lack of an effect of beneficiaries on reproduction and vegetative performance suggests that the interaction between L. acaulis and its beneficiaries is probably commensalistic.

Advances in Dendrobium molecular research: Applications in genetic variation, identification and breeding.

Orchids of the genus Dendrobium are of great economic importance in global horticultural trade and in Asian traditional medicine. For both areas, research yielding solid information on taxonomy, phylogeny, and breeding of this genus are essential. Traditional morphological and cytological characterization are used in combination with molecular results in classification and identification. Markers may be useful when used alone but are not always reliable in identification. The number of species studied and identified by molecular markers is small at present. Conventional breeding methods are time-consuming and laborious. In the past two decades, promising advances have been made in taxonomy, phylogeny and breeding of Dendrobium species due to the intensive use of molecular markers. In this review, we focus on the main molecular techniques used in 121 published studies and discuss their importance and possibilities in speeding up the breeding of new cultivars and hybrids.

What´s in the tank? Nematodes and other major components of the meiofauna of bromeliad phytotelms in lowland Panama.

BACKGROUND: Nematodes are a very diverse and extremely abundant group of animals, but their occurrence in the tropics is surprisingly little understood. We investigated the meiofauna of epiphytic tank bromeliads in the lowlands of Panama with particular emphasis on nematodes. RESULTS: We encountered 89 morphospecies of nematodes in 54 bromeliad tanks, which were sampled in the wet and the dry season. Rotifers were by far the most abundant group in both the dry and the wet season (with up to 960 individual ml(-1)), followed by nematodes, annelids and harpacticoid copepods. Individual plants hosted up to 25 nematode species. These nematodes represented a diversity of feeding guilds, suction-feeders and deposit-feeders being most abundant. The relative abundances of feeding-types of nematodes differed considerably in the wet and dry season. Both species richness and abundance were strongly correlated with the size of the phytotelms and the season, while species diversity assessed with the Shannon-index was affected by neither of the two. CONCLUSION: This is the first study with a particular focus on the diversity of nematodes in tank bromeliads. We document a meiofauna of considerable abundance and diversity, which suggests important functional roles in ecological processes such as decomposition, which in turn warrants further study.

Photoprotection related to xanthophyll cycle pigments in epiphytic orchids acclimated at different light microenvironments in two tropical dry forests of the Yucatan Peninsula, Mexico.

MAIN CONCLUSION: Epiphytic orchids from dry forests of Yucatán show considerable photoprotective plasticity during the dry season, which depends on leaf morphology and host tree deciduousness. Nocturnal retention of antheraxanthin and zeaxanthin was detected for the first time in epiphytic orchids. In tropical dry forests, epiphytes experience dramatic changes in light intensity: photosynthetic photon flux density may be up to an order of magnitude higher in the dry season compared to the wet season. To address the seasonal changes of xanthophyll cycle (XC) pigments and photosynthesis that occur throughout the year, leaves of five epiphytic orchid species were studied during the early dry, dry and wet seasons in a deciduous and a semi-deciduous tropical forests at two vertical strata on the host trees (3.5 and 1.5 m height). Differences in XC pigment concentrations and photosynthesis (maximum quantum efficiency of photosystem II; F v/F m) were larger among seasons than between vertical strata in both forests. Antheraxanthin and zeaxanthin retention reflected the stressful conditions of the epiphytic microhabitat, and it is described here in epiphytes for the first time. During the dry season, both XC pigment concentrations and photosystem II heat dissipation of absorbed energy increased in orchids in the deciduous forest, while F v/F m and nocturnal acidification (ΔH(+)) decreased, clearly as a response to excessive light and drought. Concentrations of XC pigments were higher than those in orchids with similar leaf shape in semi-deciduous forest. There, only Encyclia nematocaulon and Lophiaris oerstedii showed somewhat reduced F v/F m. No changes in ΔH(+) and F v/F m were detected in Cohniella ascendens throughout the year. This species, which commonly grows in forests with less open canopies, showed leaf tilting that diminished light interception. Light conditions in the uppermost parts of the canopy probably limit the distribution of epiphytic orchids and the retention of zeaxanthin can help to cope with light and drought stress in these forests during the dry season.

A cool experimental approach to explain elevational treelines, but can it explain them?

At alpine treeline, trees give way to low-stature alpine vegetation. The main reason may be that tree canopies warm up less in the sun and experience lower average temperatures than alpine vegetation. Low growth temperatures limit tissue formation more than carbon gain, but whether this mechanism universally determines potential treeline elevations is the subject of debate. To study low-temperature limitation in two contrasting treeline tree species, Fajardo and Piper (American Journal of Botany 101: 788-795) grew potted seedlings at ground level or suspended at tree-canopy height (2 m), introducing a promising experimental method for studying the effects of alpine-vegetation and tree-canopy microclimates on tree growth. On the basis of this experiment, the authors concluded that lower temperatures at 2 m caused carbon limitation in one of the species and that treeline-forming mechanisms may thus be taxon-dependent. Here we contest that this important conclusion can be drawn based on the presented experiment, because of confounding effects of extreme root-zone temperature fluctuations and potential drought conditions. To interpret the results of this elegant experiment without logistically challenging technical modifications and to better understand how low temperature leads to treeline formation, studies on effects of fluctuating vs. stable temperatures are badly needed. Other treeline research priorities are interactions between temperature and other climatic factors and differences in microclimate between tree canopies with contrasting morphology and physiology. In spite of our criticism of this particular study, we agree that the development of a universal treeline theory should include continuing explorations of taxon-specific treeline-forming mechanisms.

'Hemiepiphyte': a confusing term and its history.

BACKGROUND AND SCOPE: Over more than 120 years of scientific study since Schimper's seminal work, the recognized categories of structurally dependent plants have changed several times. Currently, ignoring parasitic mistletoes, it is usual to distinguish four functional groups: (1) true epiphytes; (2) primary hemiepiphytes; (3) secondary hemiepiphytes; and (4) climbing plants, i.e. lianas and vines. In this Viewpoint, it is argued that the term secondary hemiepiphytes (SHs) is misleading, that its definition is hard to impossible to apply in the field and, possibly causally related to this conceptual problem, that the use of this category in field studies is inconsistent, which now hampers interpretation and generalization. CONCLUSIONS: Categories will frequently fail to capture gradual biological variation, but terms and concepts should be as unambiguous as possible to facilitate productive communication. A detailed analysis of the conceptual problems associated with the term SH and its application in scientific studies clearly shows that this goal is not fulfilled in this case. Consequently, the use of SH should be abandoned. An alternative scheme to categorize structurally dependent flora is suggested.

Altitudinal changes in temperature responses of net photosynthesis and dark respiration in tropical bryophytes.

BACKGROUND AND AIMS: There is a conspicuous increase of poikilohydric organisms (mosses, liverworts and macrolichens) with altitude in the tropics. This study addresses the hypothesis that the lack of bryophytes in the lowlands is due to high-temperature effects on the carbon balance. In particular, it is tested experimentally whether temperature responses of CO(2)-exchange rates would lead to higher respiratory carbon losses at night, relative to potential daily gains, in lowland compared with lower montane forests. METHODS: Gas-exchange measurements were used to determine water-, light-, CO(2)- and temperature-response curves of net photosynthesis and dark respiration of 18 tropical bryophyte species from three altitudes (sea level, 500 m and 1200 m) in Panama. KEY RESULTS: Optimum temperatures of net photosynthesis were closely related to mean temperatures in the habitats in which the species grew at the different altitudes. The ratio of dark respiration to net photosynthesis at mean ambient night and day temperatures did not, as expected, decrease with altitude. Water-, light- and CO(2)-responses varied between species but not systematically with altitude. CONCLUSIONS: Drivers other than temperature-dependent metabolic rates must be more important in explaining the altitudinal gradient in bryophyte abundance. This does not discard near-zero carbon balances as a major problem for lowland species, but the main effect of temperature probably lies in increasing evaporation rates, thus restricting the time available for photosynthetic carbon gain, rather than in increasing nightly respiration rates. Since optimum temperatures for photosynthesis were so fine tuned to habitat temperatures we analysed published temperature responses of bryophyte species worldwide and found the same pattern on the large scale as we found along the tropical mountain slope we studied.